Psychological, social and sexual consequences of female genital mutilation/cutting (FGM/C): a systematic review of quantitative studies
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Psychological, social and sexual consequences of female genital mutilation/cutting (FGM/C): a systematic review of quantitative studies Report from Kunnskapssenteret (Norwegian Knowledge Centre for the Health Services) No 13–2010 Systematic review Background: In November 2008, the Norwegian Knowledge Centre for Violence and Traumatic Stress Studies (NKVTS) commissioned the Norwegian Knowledge Centre for the Health Services (NOKC) to conduct a systematic review about the consequences of female genital mutilation/cutting (FGM/C).The review would answer the question: What are the psychological, social and sexual consequences of FGM/C? Methods: We searched systematically for relevant literature in international scientific da- tabases, in databases of international organisations that are engaged in aspects related to FGM/C, and in reference lists of relevant reviews and included studies. We also communicated with professionals working with FGM/C related issues. We selected studies according to pre-specified criteria, appraised the methodolo- gical quality using checklists, and summarized the study level results using ta- bles and calculated effect estimates (risk ratio and mean difference) in addition to performing meta-analyses to estimate effect. We applied the instrument GRA- DE to assess the extent to which we could have confidence in the effect estima- tes. Results: We included and summarized results from 17 comparative (continued)
Norwegian Knowledge Centre for the Health Services (Kunnskapssenteret)
PO Box 7004, St. Olavs plass
N-0130 Oslo
(+47) 23 25 50 00
www.kunnskapssenteret.no
Report: ISBN ISBN 978-82-8121-350-0 ISSN 1890-1298
no 13–2010
studies with a total of 12,755 participants from communities
(continued from page one)
where FGM/C is practiced. All studies compared women with FGM/C to women
without FGM/C. The evidence base was insufficient to draw conclusions about
the psychological and social consequences of FGM/C. The effect estimates show
that compared to women without FGM/C women with FGM/C are more likely
to experience 1) pain during intercourse, 2) reduced sexual satisfaction, and 3)
reduced sexual desire. However, the quality of the evidence was too low to draw
conclusions about a causal relationship between FGM/C and psychological, so-
cial and sexual consequences. Conclusion: There is a paucity of high quality
evidence regarding the consequences of FGM/C. While the evidence base is in-
sufficient to draw causal conclusions about the consequences of FGM/C, our
results show that women with FGM/C experience pain and reduction in sexual
satisfaction and desire compared to women without FGM/C.Title Psychological, social and sexual consequences of female genital
mutilation/cutting (FGM/C): a systematic review of quantitative studies
Norwegian title Psykiske, sosiale og seksuelle konsekvenser av kjønnslemlestelse: en
systematisk oversikt over kvantitative studier
Institution Nasjonalt kunnskapssenter for helsetjenesten
(Norwegian Knowledge Centre for the Health Services)
John-Arne Røttingen, director
Authors Berg, Rigmor C, researcher
Denison, Eva, researcher (project leader)
Fretheim, Atle, research director (project responsible)
ISBN 978-82-8121-350-0
ISSN 1890-1298
Report nr 13 – 2010
Project nr 518
Type of report Systematic review
No. of pages 68 (77 appendices included)
Client Norwegian Centre for Violence and Traumatic Stress Studies
(Nasjonalt kunnskapssenter om vold og traumatisk stress)
Keywords Female genital mutilation / cutting, consequences, psychological,
social, sexual
Citation Berg RC, Denison E, Fretheim A. Psychological, social and sexual
consequences of female genital mutilation/cutting (FGM/C): a
systematic review of quantitative studies. Report from
Kunnskapssenteret nr 13−2010. Oslo: Nasjonalt kunnskapssenter for
helsetjenesten, 2010.
Norwegian Knowledge Centre for the Health Services summarizes and
disseminates evidence concerning the effect of treatments, methods,
and interventions in health services, in addition to monitoring health
service quality. Our goal is to support good decision making in order to
provide patients in Norway with the best possible care. The Centre is
organized under The Directorate of Health, but is scientifically and
professionally independent. The Centre has no authority to develop
health policy or responsibility to implement policies.
We would like to thank R. Elise Johansen, Susan Munabi-
Babigumira, Tove Ringerike and an anonymous reviewer for their
expertise in this project. Norwegian Knowledge Centre for the Health
Services assumes final responsibility for the content of this report.
Norwegian Knowledge Centre for the Health Services
Oslo, June 2010
1List of abbreviations
DHS Demographic and Health Survey.
DSM-IV Diagnostic and Statistical Manual of Mental Disorders, 4th ed.
FGM/C Female Genital Mutilation/Cutting.
FSFI Female Sexual Function Index.
NKVTS Nasjonalt kunnskapssenter om vold og traumatisk stress /
Norwegian Centre for Violence and Traumatic Stress Studies.
NOKC Nasjonalt kunnskapssenter for helsetjenesten / Norwegian
Knowledge Centre for the Health Services.
PRB Population Reference Bureau.
PTSD Post traumatic stress disorder.
UNFPA United Nations Population Fund.
UNICEF United Nations Children's Fund.
WHO World Health Organization.
2 List of abbreviationsKey messages Psychological, social and sexual consequences of female genital mutila- tion/cutting (FGM/C): a systematic review of quantitative studies Background: In November 2008, the Norwegian Knowledge Centre for Violence and Traumatic Stress Studies (NKVTS) commissioned the Norwegian Knowledge Centre for the Health Services (NOKC) to conduct a systematic review about the consequences of female genital mutilation/cutting (FGM/C). The review would an- swer the question: What are the psychological, social and sexual consequences of FGM/C? Methods: We searched systematically for relevant literature in international scien- tific databases, in databases of international organisations that are engaged in as- pects related to FGM/C, and in reference lists of relevant reviews and included stud- ies. We also communicated with professionals working with FGM/C related issues. We selected studies according to pre-specified criteria, appraised the methodological quality using checklists, and summarized the study level results using tables and cal- culated effect estimates (risk ratio and mean difference) in addition to performing meta-analyses to estimate effect. We applied the instrument GRADE to assess the extent to which we could have confidence in the effect estimates. Results: We included and summarized results from 17 comparative studies with a total of 12,755 participants from communities where FGM/C is practiced. All studies compared women with FGM/C to women without FGM/C. The evidence base was insufficient to draw conclusions about the psychological and social consequences of FGM/C. The effect estimates show that compared to women without FGM/C women with FGM/C are more likely to experience 1) pain during intercourse, 2) re- duced sexual satisfaction, and 3) reduced sexual desire. However, the quality of the evidence was too low to draw conclusions about a causal relationship between FGM/C and psychological, social and sexual consequences. Conclusion: There is a paucity of high quality evidence regarding the consequences of FGM/C. While the evidence base is insufficient to draw causal conclusions about the consequences of FGM/C, our results show that women with FGM/C experience pain and reduction in sexual satisfaction and desire compared to women without FGM/C. 3 Key messages
Executive summary BACKGROUND Female genital mutilation/cutting (FGM/C) is a traditional practice that involves "the partial or total removal of the female external genitalia or other injury to the female genital organs for cultural or other non-therapeutic reasons." FGM/C is prac- tised in more than 28 countries in Africa and in some countries in the Middle East and Asia. Although limited data exist, it is speculated that FGM/C is practised by immigrant communities in a number of other countries, including Australia, Can- ada, France, New Zealand, Norway, Sweden, Switzerland, the United Kingdom, and the United States. The practice of FGM/C is rooted in social conventions within a frame of psycho-sexual and social reasons such as control of women's sexuality and family honour which is enforced by community mechanisms. FGM/C is recognized as a harmful practice which abrogates human rights. It is pro- hibited by law in several African and Western countries. The current WHO classifi- cation describes four types of FGM/C: Type I, clitoridectomy, involves partial or to- tal removal of the clitoris and/or the prepuce. Type II, excision, involves partial or total removal of the clitoris and the labia minora, with or without excision of the la- bia majora. Type III, infibulation, involves narrowing of the vaginal orifice with creation of a covering seal by cutting and appositioning the labia minora and/or the labia majora, with or without excision of the clitoris. Type IV, other, involves all other harmful procedures to the female genitalia for non-medical purposes, for ex- ample: pricking, piercing, incising, scraping, and cauterization. There is great varia- tion in prevalence, reflecting ethnicity, tradition and sociodemographic factors. Countries with very high prevalence, over 70%, include Egypt, Ethiopia, Mali, and Somalia. FGM/C is associated with several health risks such as severe pain, bleed- ing, shock, infections, and difficulty in passing urine and faeces. Caesarean section, blood loss and increased perinatal mortality are associated birth risks. Non-medical consequences from FGM/C are less clear. We asked the following question: What are the psychological, social and sexual con- sequences of FGM/C? 4 Executive summary
METHODS We searched systematically for literature in the following scientific databases: Afri- can Index Medicus, Anthropology Plus, British Nursing Index and Archive, The Cochrane Library (CENTRAL, Cochrane Database of Systematic Reviews, Database of Abstracts of Reviews of Effects), EMBASE, EPOC, MEDLINE, PILOTS, POPLINE, PsychINFO, Social Services Abstracts, Sociological Abstracts, and WHOLIS. We also searched in databases of international organisations that are engaged in research concerning FGM/C, manually in reference lists of relevant reviews and studies in- cluded in this systematic review, as well as communicated with experts engaged in FGM/C related work. We searched for studies that used the following study designs: systematic reviews, cohort studies, case-control studies, and cross-sectional studies. Two of the authors independently assessed studies for inclusion according to pre- specified criteria and considered the methodological quality of the studies using checklists. We summarized the study level results in text and tables and calculated effect estimates (relative risk and mean difference). We also performed meta- analyses to estimate effect, using Mantel-Haenszel random effects meta-analyses for dichotomous outcomes and inverse variance random effects meta-analyses for con- tinuous outcomes. We applied the instrument GRADE to assess the extent to which we could have confidence in the effect estimates. RESULTS We identified 3,669 publications and after having assessed titles, abstracts, and arti- cles in full text we included 17 studies that fulfilled the inclusion criteria. All in- cluded studies were observational comparative studies (15 cross-sectional studies and 2 case-control studies) that compared women who had been subjected to FGM/C with women who had not been subjected to FGM/C. We failed to obtain two potentially relevant records, despite extensive retrieval efforts. We arrived upon a final decision of low study quality for ten of the 17 studies, mod- erate quality for five and high quality for two. In our assessment, using the GRADE instrument, the quality of the evidence was very low with regards to documenting a causal relationship between FGM/C and psychological, social and sexual conse- quences. Collectively, the studies involved a total of 12,755 participants from nine different countries. One study was from Israel, one was from Saudi Arabia, while the remaining fifteen studies were from countries in Africa: Central African Republic, Egypt, Gambia, Ghana, Nigeria, Senegal, and Sudan. Four studies reported on psychological consequences. Study level results suggested that women with FGM/C may be more likely than women without FGM/C to experi- ence psychological disturbances (have a psychiatric diagnosis, suffer from anxiety, somatisation, phobia, and low self-esteem). However, our meta-analyses for anxiety, somatisation, depression, and hostility failed to reach significance and were marred by high heterogeneity. We were unable to draw solid conclusions concerning psycho- 5 Executive summary
logical consequences. Only two studies, both of low study quality, included some measure of social consequences of FGM/C and we were unable to draw any conclu- sions. Concerning sexual consequences, several studies were sufficiently similar to warrant pooling of effect sizes in meta-analysis for the outcomes pain during inter- course, satisfaction, desire, initiation of sex, orgasm, reporting clitoris as the most sensitive area of the body, and reporting the breasts as the most sensitive areas of the body. Compared to women without FGM/C, women with FGM/C were 1.5 times more likely to experience pain during intercourse (RR= 1.52, 95%CI= 1.15, 2.0). The pooled effect estimate from two studies suggested that women with FGM/C experi- ence significantly less sexual satisfaction (St.mean diff= -0.34, 95%CI= -0.56, -0.13). Women with FGM/C were twice as likely to report that they did not experience sex- ual desire (RR= 2.15, 95%CI= 1.37, 3.36). These meta-analysis results were sup- ported by other study level findings. The results of the remaining meta-analyses were marred by high heterogeneity and the results were inconclusive. Collectively, the results provide evidence that women with FGM/C are more likely to experience pain during intercourse, reduced sexual satisfaction and reduced sexual desire than women without FGM/C, but the low quality of the body of evidence precludes us from drawing conclusions regarding causality. CONCLUSION The psychological, social and sexual consequences of FGM/C is an under-researched and neglected issue. The low quality of the body of evidence precludes us from draw- ing conclusions regarding causality, and the evidence base is insufficient to draw solid conclusions about the psychological and social consequences of FGM/C. How- ever, our results substantiate the proposition that a woman whose genital tissues have been partly removed is more likely to experience increased pain and reduction in sexual satisfaction and desire. Future studies investigating the consequences of FGM/C should compare clearly defined groups that differ by the extent of FGM/C, whereby classification is based on gynaecological examination. Multi-centre, com- parative studies which apply a methodology that increases the likelihood of equiva- lency of exposed and unexposed groups of women and standardized data collection, are preferable. The Norwegian Knowledge Centre for the Health Services summarizes and disseminates evidence concerning the effect of treatments, methods, and interventions in health services, in addition to monitoring health service quality. Our goal is to support good decision making in order to provide patients in Norway with the best possible care. The Centre is organized under The Directorate of Health, but is scientifically and professionally independent. The Centre has no authority to develop health policy or responsibility to implement policies. Norwegian Knowledge Centre for the Health Services PB 7004 St. Olavs plass N-0130 Oslo, Norway 6 Executive summary
Telephone: +47 23 25 50 00 E-mail: post@kunnskapssenteret.no Full report (pdf): www.kunnskapssenteret.no 7 Executive summary
1-side oppsummering (norsk) Bakgrunn: I november 2008 gav Nasjonalt kunnskapssenter om vold og trauma- tisk stress (NKVTS) i oppdrag til Nasjonalt kunnskapssenter for helsetjenesten (NOKC) å utføre en systematisk kunnskapsoppsummering om konsekvensene av kjønnslemlestelse. Oppsummeringen skulle besvare spørsmålet: Hva er de psykiske, sosiale og seksuelle konsekvensene av kjønnslemlestelse? Metode: Vi søkte systematisk etter relevant litteratur i internasjonale databaser, i databaser til internasjonale organisasjoner som driver prosjekter om kjønnslemles- telse, i referanselistene til relevante kunnskapsoversikter og de inkluderte studiene, og kommuniserte med eksperter som arbeider med kjønnslemlestelse. Vi valgte ut studier som oppfylte våre predefinerte inklusjonskriterier. Vi brukte sjekklister for å vurdere den metodiske kvaliteten til studiene og vurderte den samlede dokumenta- sjonen for endepunktene ved hjelp av GRADE. Vi oppsummerte resultater på stu- dienivå i tabeller og beregnet effektestimat (relativ risiko og gjennomsnittsforskjell) samt utførte meta-analyser hvor vi mente dette var metodologisk forsvarlig. Resultater: Vi inkluderte og oppsummerte resultatene for 17 observasjonsstudier som sammenlignet kvinner utsatt for kjønnslemlestelse med kvinner uten kjønns- lemlestelse. Til sammen deltok 12,755 kvinner. Av de 17 inkluderte studiene ble 10 vurdert til å ha lav metodologisk kvalitet. Vi vurderte den samlede dokumentasjonen for endepunktene ved hjelp av GRADE som viste at dokumentasjonen hadde svært lav kvalitet, som innebærer at effektestimatet er for usikkert til at vi kan trekke noen kausale slutninger. Resultatene viser at kvinner med kjønnslemlestelse har større risiko for å oppleve 1) smerte under samleie, 2) nedsatt seksuell tilfredshet, og 3) nedsatt seksuell lystfølelse, sammenlignet med kvinner uten kjønnslemlestelse. Konklusjon: Det mangler dokumentasjon av høy kvalitet når det gjelder konse- kvenser av kjønnslemlestelse. Kunnskapsgrunnlaget er utilstrekkelig for å dra sikre konklusjoner angående psykiske og sosiale konsekvenser. Resultatene viser at kvin- ner med kjønnslemlestelse i større grad opplever seksuelle problemer enn kvinner uten kjønnslemlestelse, men også her er kunnskapsgrunnlaget utilstrekkelig og av for lav kvalitet til at vi kan konkludere at det er en direkte årsakssammenheng. 8 1-side oppsummering (norsk)
Sammendrag (norsk) BAKGRUNN Kjønnslemlestelse er en tradisjonell praksis som innebærer at hele eller deler av de eksterne kvinnelige kjønnsorganene fjernes eller skades av ikke-terapeutiske grun- ner. Kjønnslemlestelse praktiseres i mer enn 28 land i Afrika, i noen land i Midtøs- ten og Asia, og muligens i immigrantsamfunn i vestlige land som Australia, Canada, Frankrike, Norge, New Zealand, Storbritannia, Sveits, Sverige, og USA. Kjønnslem- lestelse er grunnet i kulturelle og sosiale forestillinger, der kontroll av kvinnelig sek- sualitet og vern av familiens ære er viktige normer. Kjønnslemlestelse er anerkjent som en skadelig praksis som krenker menneskelige rettigheter og er uttrykkelig for- budt i mange afrikanske og vestlige land. Kjønnslemlestelse klassifiseres i fire kate- gorier: Type I, klitoridektomi, delvis eller total fjerning av klitoris og/eller forhuden; Type II, eksisjon, delvis eller total fjerning av klitoris og de små kjønnsleppene; Type III: infibulasjon, delvis eller fullstendig fjerning av ytre kjønnslepper og gjensying slik at urinrørsåpningen dekkes av et hudseil og skjedeåpningen forsnevres til ca. 1 cm i diameter; Type IV: alle andre former, inklusive prikking og stikking i klitoris, strekking av klitoris og/eller kjønnslepper, etsning eller brenning av klitoris og om- liggende vev, og innføring av etsende stoffer i skjeden for å minske hulrommets stør- relse. Forekomsten av kjønnslemlestelse i Afrika varierer sterkt, avhengig av kulturelle, etniske, sosiale og demografiske forhold. Land med meget høy forekomst, over 70 %, er for eksempel Egypt, Etiopia, Mali, og Somalia. Kjønnslemlestelse settes i sam- menheng med flere helsefarer som for eksempel alvorlige smerter, blødning, sjokk, vanskeligheter med urinering og avføring, samt infeksjoner. Keisersnitt, blodtap og økt perinatal dødelighet er risikofaktorer i sammenheng med fødsel. Det fins mindre forskning angående andre konsekvenser av kjønnslemlestelse. Vi stilte følgende spørsmål: Hva er de psykiske, sosiale og seksuelle konsekvensene av kjønnslemlestelse? METODE Vi søkte systematisk etter relevant litteratur i følgende 13 internasjonale databaser: African Index Medicus, Anthropology Plus, British Nursing Index and Archive, The Cochrane Library (CENTRAL, Cochrane Database of Systematic Reviews, Database of Abstracts of Reviews of Effects), EMBASE, EPOC, MEDLINE, PILOTS, POPLINE, 9 1-side oppsummering (norsk)
PsychINFO, Social Services Abstracts, Sociological Abstracts, og WHOLIS. Vi søkte også i databaser til internasjonale organisasjoner som driver prosjekter om kjønns- lemlestelse, i referanselistene til relevante kunnskapsoversikter og de inkluderte studiene, og kommuniserte med eksperter som arbeider med kjønnslemlestelse. Vi søkte etter litteratur med følgende studiedesign: systematiske kunnskapssoversikter, kohortestudier, kasuskontrollstudier, og tverrsnittsstudier. Vi valgte ut studier som oppfylte våre predefinerte inklusjonskriterier. Deretter brukte vi sjekklister for å vurdere den metodiske kvaliteten til studiene. Vi oppsum- merte resultater på studienivå i tabeller og beregnet effektestimat (relativ risiko og gjennomsnittsforskjell) samt utførte meta-analyser hvor vi mente dette var metodo- logisk forsvarlig. Vi vurderte den samlede dokumentasjonen for endepunktene ved hjelp av GRADE. RESULTAT Vi identifiserte 3669 publikasjoner og etter å ha vurdert titler, sammendrag og artik- ler i fulltekst fant vi 17 studier som oppfylte inklusjonskriteriene. Alle studiene var observasjonsstudier (15 tverrsnittstudier og 2 kasuskontrollstudier) som sammen- lignet kvinner utsatt for kjønnslemlestelse med kvinner uten kjønnslemlestelse. To mulig relevante publikasjoner fikk vi ikke tak i, på tross av omfattende forsøk. Av de 17 inkluderte studiene ble 10 vurdert til å ha lav metodologisk kvalitet. Vi vur- derte kvaliteten på den samlede dokumentasjonen for endepunktene ved hjelp av GRADE til svært lav. Det betyr at effektestimatet er for usikkert til å kunne doku- mentere en kausal sammenheng mellom kjønnslemlestelse og psykiske, sosiale og seksuelle konsekvenser. Til sammen deltok 12 755 kvinner i de 17 studiene, som var utført i ni ulike land. Én studie var fra Israel, én var fra Saudi Arabia, og de andre 15 studiene var fra land i Afrika: Den Sentralafrikanske republikk, Egypt, Gambia, Ghana, Nigeria, Senegal, og Sudan. Fire studier inkluderte psykiske utfallsmål. Resultater på studienivå tydet på at kvinner med kjønnslemlestelse kan ha større risiko for å oppleve psykiske problemer (inneha psykiatrisk diagnose, lide av angst, somatisering, fobi, lav selvfølelse). Men meta-analyse resultatene for angst, somatisering, depresjon, og fiendtlighet viste ikke signifikante forskjeller og høy heterogenitet tilsa uforenlighet mellom studiene. Vi kunne ikke trekke solide konklusjoner for psykiske konsekvenser. Kun to studier, med lav studiekvalitet, inkluderte sosiale utfallsmål og vi kunne ikke trekke noen konklusjoner. I forhold til seksuelle konsekvenser var flere studier tilstrekkelig like til at vi kunne utføre meta-analyser. Vi utførte meta-analyser for syv utfallsmål: smerte under samleie, seksuell tilfredshet, lystfølelse, ta initiativet til sex, orgasme, mene at klitoris er den mest følsomme delen av kroppen, mene at brystene er de mest følsomme delene av kroppen. Sammenlignet med kvinner uten kjønnslemles- telse var kvinner med kjønnslemlestelse 1.5 ganger mer utsatt for smerte under sam- leie (RR= 1,52, 95 % CI= 1,15 til 2,0). Resultatet fra to studier viste at kvinner med kjønnslemlestelse opplever mindre seksuell tilfredshet (St.mean diff= -0,34, 95 % CI 10 1-side oppsummering (norsk)
-0,56 til -0,13) enn kvinner uten kjønnslemlestelse. Kvinner med kjønnslemlestelse var mer enn to ganger så utsatt for ikke å oppleve seksuell lystfølelse (RR= 2,15, 95 % CI= 1,37 til 3,36). Lignende resultater på studienivå støttet disse funnene. Det var høy heterogenitet i de andre meta-analysene og resultatene var ikke entydige. Til sammen viser disse resultatene at kvinner med kjønnslemlestelse i større grad opp- lever seksuelle problemer enn kvinner uten kjønnslemlestelse, men kunnskaps- grunnlaget er for svakt til at vi kan slå fast at dette er en direkte følge av kjønnslem- lestelse. KONKLUSJON Det fins lite forskning om de psykiske, sosiale og seksuelle konsekvensene av kjønns- lemlestelse. Kunnskapsgrunnlaget er utilstrekkelig for å dra sikre konklusjoner an- gående psykiske og sosiale konsekvenser, men resultatene fra denne studien viser at kvinner som har vært utsatt for kjønnslemlestelse er mer utsatt for seksuelle prob- lemer, slik som smerte under samleie, og redusert seksuell tilfredshet og lystfølelse. Kunnskapsgrunnlaget er utilstrekkelig og av for lav kvalitet til å dra kausale slut- ninger. For å få mer sikker kunnskap er det behov for ytterligere studier. Slike studi- er bør sikre at gruppene av kvinner med og uten kjønnslemlestelse er sammenlign- bare, at forekomst og grad av kjønnslemlestelse er målt ved fysisk undersøkelse, og at standardiserte datainnsamlingsmetoder blir brukt. 11 1-side oppsummering (norsk)
Table of contents
LIST OF ABBREVIATIONS 2
KEY MESSAGES 3
EXECUTIVE SUMMARY 4
Background 4
Methods 5
Results 5
Conclusion 6
1-SIDE OPPSUMMERING (NORSK) 8
SAMMENDRAG (NORSK) 9
Bakgrunn 9
Metode 9
Resultat 10
Konklusjon 11
TABLE OF CONTENTS 12
PREFACE 14
OBJECTIVE 15
BACKGROUND 16
Classifications 16
Prevalence 17
Interventions to reduce the prevalence of FGM/C 18
Consequences 19
Physical consequences 20
Other consequences 21
Psychological consequences 21
Social consequences 21
Sexual consequences 22
METHOD 24
Literature search 24
Inclusion criteria 25
Exclusion criteria 25
12Selection of studies 26
Data extraction and analysis 26
RESULTS 28
Description of included literature 28
Results of the search 28
Description of included studies 29
Study design and sample recruitment 32
Population 32
Outcomes 35
Measurement 36
Quality assessment 36
Consequences of FGM/C 37
Psychological consequences of FGM/C 37
Results of meta-analyses for psychological consequences 39
Social consequences of FGM/C 40
Sexual consequences of FGM/C 40
Results of meta-analyses for sexual consequences 43
Dyspareunia 43
Satisfaction 44
No sexual desire 45
Never initiate sex 45
No orgasm 46
Clitoris most sensitive area of the body 46
Breasts most sensitive area of the body 47
Additional syntheses of results across studies 47
DISCUSSION 49
Discussion of main results 49
Psychological consequences 49
Social consequences 50
Sexual consequences 50
Quality of the evidence 55
Strengths and limitations 58
CONCLUSIONS 60
Need for further research 60
REFERENCES 62
APPENDICES 69
1. Search for literature 69
2. Excluded studies 73
3. Quality assessment 74
4. GRADE 76
13Preface In November 2008, the Norwegian Knowledge Centre for Violence and Traumatic Stress Studies (NKVTS) contacted the Norwegian Knowledge Centre for the Health Services (NOKC) with a request for assistance in establishing a competence centre on the topic of FGM/C. Specifically, the NKVTS commissioned the NOKC to conduct a series of systematic reviews about female genital mutilation/cutting (FGM/C), one of which assessed the psychological, social and sexual consequences of FGM/C. One systematic review, about the effectiveness of interventions designed to reduce the prevalence of FGM/C, is published (1). Another systematic review, about the factors promoting and hindering the practice, is underway, and a third, delineating extant guidelines regarding FGM/C will likely be completed by the end of 2010. The project team was composed of: • Project coordinator, researcher, Eva Denison, NOKC • Researcher, Rigmor C Berg, NOKC • Research director, Atle Fretheim, NOKC Additionally, the literature search was conducted by research librarian Sari Orm- stad, and Jan Odgaard-Jensen provided statistical guidance. Both are with the NOKC. We are grateful for peer review by two internal and two external reviewers: • Susan Munabi-Babigumira, researcher, NOKC • Tove Ringerike, researcher, NOKC • R. Elise Johansen, Technical officer at World Health Organization, Geneva • Anonymous reviewer The aim of this report is to support well-informed decisions in health promotion that inform the work to reduce the prevalence of FGM/C and improve quality of services related to FGM/C. The evidence should be considered together with other relevant issues, such as clinical experience and patient preferences. Anne Karin Lindahl Atle Fretheim Eva Denison Director Research Director Project coordinator 14 Preface
Objective This systematic review summarizes published, empirical quantitative data describ- ing the psychological, social and sexual consequences of FGM/C. NKVTS commissioned the NOKC to conduct a systematic review to support the or- ganization’s health promotion work concerning FGM/C among women subjected to and at risk for the practice in Norway, but the systematic review is of relevance in all countries where FGM/C may occur. The overall aim of the systematic review is to support well-informed decisions in health promotion that inform work to reduce the prevalence of FGM/C and improve quality of services related to FGM/C. The main research question was: • What are the psychological, social and sexual consequences of FGM/C? 15 Objective
Background The terminology used for the cutting of external female genital tissues varies. It has been referred to as "female circumcision", "female genital mutilation", "female geni- tal cutting" and "female genital mutilation/cutting" (2). We adopt the official termi- nology used by UNICEF and UNFPA "female genital mutilation/cutting" (FGM/C) throughout this report. FGM/C is a traditional practice that involves "the partial or total removal of the female external genitalia or other injury to the female genital organs for cultural or other non-therapeutic reasons" (3). Although FGM/C transcends geography, it is primarily practised among various ethnic groups in more than 28 countries in Africa, usually on girls under the age of 15 years. The practise is also found in some countries in the Middle East and Asia (4;5), for example among some Bedouin tribes in the western part of Saudi Arabia (6). Although limited data exist, it is speculated that FGM/C is practised by immi- grant communities in a number of other countries, including Australia, Canada, France, New Zealand, Norway, Sweden, Switzerland, the United Kingdom, and the United States (4). Unlike male circumcision, which provides some protection from certain infections, such as urinary tract infections and human immunodeficiency virus (7;8), there are no known health benefits to FGM/C (2). CLASSIFICATIONS To clarify understanding of the prevalence and consequences of FGM/C, WHO has classified the procedure into four categories: Type I, clitoridectomy, involves partial or total removal of the clitoris and/or the prepuce. Type II, excision, involves partial or total removal of the clitoris and the labia minora, with or without excision of the labia majora. Type III, infibulation, involves narrowing of the vaginal orifice with creation of a covering seal by cutting and appositioning the labia minora and/or the labia majora, with or without excision of the clitoris. Infibulation is considered the most invasive type of FGM/C. Defibulation, opening of the covering seal, is often necessary prior to childbirth. Reinfibulation refers to the recreation of an infibula- tion after defibulation. Type IV, other, involves all other harmful procedures to the female genitalia for non-medical purposes, for example: pricking, piercing, incising, scraping, and cauterizing (2). In type IV, no genital tissue is excised. 16 Background
Within these classifications there is a wide range of variation, not yet systematically studied and documented. For example, the technical variation of cutting differs within the same practitioner over time and instrumentation used, resulting in varia- tion in degrees of FGM/C (2;9). Common to all operations, except type IV proce- dures, is some degree of excision of the external genitalia, from excision of minor skin parts around the clitoris to clitoridectomy and removal of the labia. Each com- munity use the cutting of their own choice for their own reasons and beliefs. Simi- larly, various instruments are used to perform the procedure, including razor blades, glass, knives, and scissors (10). PREVALENCE Globally, it has been proposed that FGM/C type II is the most frequently practiced form, representing an estimated 80% of all procedures of FGM/C (11). While type III is thought to represent about 10% of FGM/C in Africa, it is probably the most fre- quently used type of FGM/C in some countries, including Djibouti, Somalia and northern Sudan (12). Recent national figures for African countries show a prevalence of FGM/C of more than 70% in Burkina Faso, Djibouti, Egypt, Eritrea, Ethiopia, Guinea, Mali, Mauretania, Northern Sudan, and Somalia (12). However, national rates do not re- veal the magnitude of FGM/C among certain ethnic groups; there is great variation in prevalence between and within countries, reflecting ethnicity and tradition (5). UNICEF (5) has proposed that countries be categorized in three groups according to prevalence rates. Group 1 consists of countries where prevalence rates are high (80% or more). In Group 2 countries, the prevalence rates are at intermediate levels (25- 79%) and usually only certain ethnic groups practice FGM/C, at varying levels. Group 3 countries have low prevalence rates (1-24%) and only some ethnic groups practice FGM/C. In Table 1, we present prevalence data of FGM/C among women aged 15-49 from countries which will be discussed in this systematic review and for which comparable national data exist. Table 1: Prevalence of FGM/C in selected countries Country Total prevalence Year data collected Group Central African Republic 35.6 2000 1 2 Egypt 91.0 2008 2 1 Gambia 55.0 Not stated 1 2 Ghana 5.4 2003 1 3 Nigeria 19.0 2003 2 3 Senegal 28.2 2005 1 2 Sudan 89.2 1990 2 1 Legend: 1= data from Yoder & Kahn (12). 2= data from most recent DHS survey in the country (13-15). No national data exist for Israel and Saudi Arabia, but studies document the practice among some ethnic groups in these areas. In Israel, the practice has been reported 17 Background
among particularly two ethnic groups, Ethiopian Jews and the Bedouin of southern Israel (16). However, while FGM/C was considered normative among Jews in Ethio- pia the custom appeared to be abandoned upon arrival in Israel (17). Similarly, while Bedouin women previously declared female genital surgery as an important part of their cultural identity (18), a recent study concluded that the practice had virtually disappeared among Israel's Bedouin population (19). Although indigenous to Saudi Arabia, FGM/C is currently only practiced among a few immigrant groups, Bedouin tribes and residents of the Hejaz (6). INTERVENTIONS TO REDUCE THE PREVALENCE OF FGM/C Consistent with international condemnation of FGM/C, there has been an increasing amount of initiatives geared towards the eradication of the practice among practis- ing communities. As Western governments have become more aware of FGM/C among the immigrant communities, legislation as the main intervention tool has been instituted, and European Union institutions and Member States have taken active steps towards ending FGM/C (20;21). There are now laws prohibiting FGM/C in several Western countries, including Australia, Canada, New Zealand, USA, and at least 13 countries in Western Europe (4;5). However, the implementation of anti- FGM/C laws and their impact on eliminating the practice has so far not been exten- sively studied (22). Efforts to abandon the practice of FGM/C in Africa have used several different ap- proaches, including those based on legal mechanisms, human rights frameworks, health risks, alternative rites, positive deviance, training health workers as change agents, training and converting circumcisers, and the use of comprehensive social development approaches. Interventions based on these approaches have targeted stakeholders at individual, interpersonal, community, and national levels (23). Re- cently, the Population Reference Bureau (PRB) carried out an extensive survey of current intervention projects taking place in African countries (24). In total, the PRB identified 92 projects, 27 of which were evaluated, mostly by observational designs. Only four of the 27 evaluated projects used a controlled before-and-after design, and about a dozen of the evaluations used cross-sectional or pre-post intervention ques- tionnaires or interviews without a control group. Although such surveys indicate the effectiveness of some anti-FGM/C interventions in achieving desired outcomes, such as changes in knowledge, beliefs, attitudes, be- haviours, and practices related to FGM/C (23;24), rigorous appraisal of the evidence was until recently lacking. A 2009 systematic review (1) took stock of progress to date, using rigorous methods which allowed valid assessment of intervention effects. The authors identified and included six controlled, before-and-after studies. Each study was set in a different country in Africa: Burkina Faso, Egypt, Ethiopia / Kenya, Mali, Nigeria, and Senegal. Two of the studies were directed at the individual level 18 Background
and four at the community level. The results suggested that 1) training health per- sonnel likely produced no effects in knowledge or beliefs/attitudes about FGM/C; 2) educating female students may possibly have led to a small increase in knowl- edge/awareness about FGM/C; 3) multifaceted community activities may possibly have increased the proportion of participants having favourable cognitions and in- tentions about FGM/C; 4) community empowerment through education may possi- bly have reduced prevalence of FGM/C, increased participants' knowledge about the consequences of FGM/C, and increased regrets about having had daughter cut. However, the authors warned that the low quality of the body of evidence affected the interpretation of results and raised doubts about the strength of the findings. The authors concluded that there was a paucity of high quality evidence regarding the effectiveness of interventions to reduce the prevalence of FGM/C and called for second-generation studies, which at a minimum should be of high methodological quality, focus on prevalence, and take into account regional, ethnic and sociodemo- graphic variation in the practice of FGM/C. A protocol has been submitted to the Campbell Collaboration, in which we propose to assess not only effectiveness of in- terventions, but also the extent to which intervention programs have heeded and built upon factors promoting and hindering FGM/C, the extent to which interven- tions have been provided to the most appropriate stakeholder groups, and which forces may have been overlooked as critical program elements. CONSEQUENCES FGM/C causes permanent, irreparable changes in the external female genitalia. The external female organs encompass the mons pubis, clitoris, labia minora, labia ma- jora, and vaginal opening (Figure 1). All of these organs, collectively known as the vulva, serve important sexual functions. The clitoris, with its rich supply of nerve endings, and prepuce form the most consistently erotic area of the female body (25). Sexual organs in females and males arise from the same embryologic origin. For ex- ample, the clitoris is equivalent to parts of the male penis (corpora cavernosa) (25). Further, anatomical, histological and MRI-based research has identified five sexu- ally responsive, vascular tissues of the female external genitalia: clitoris, clitoral bulbs, labia minora, urethra, and vestibule/vagina. All were found to engorge during sexual arousal, with the erectile tissue compartments (corpus cavernosum of the clitoris and corpus spongiosum of the clitoral bulbs) having the greatest change in blood volume during sexual arousal (26). Researchers have concluded that vascular tissue is important in the context of female sexual response. Operations that disrupt or potentially disrupt the female external organs, such as FGM/C, "can potentially affect sexual functioning by ablating some or all of the genital organs, or their inner- vation" (26) as well as damage neural innervation (27). In effect, with FGM/C, some fundamental structures for sexual stimulation and orgasm have been excised, al- though not all. In contrast to male circumcision where the foreskin is cut off from the tip of the penis without damaging the organ itself, the degree of cutting and 19 Background
likely harm in FGM/C is anatomically much more extensive (28) (with the possible exception of variations of type IV, such as pricking and stretching). Figure 1: Female external genitalia Physical consequences Girls exposed to FGM/C are at risk of immediate physical consequences such as se- vere pain, bleeding, shock, difficulty in passing urine and faeces, and infections. Long term consequences can include chronic pain and infections. In general, the consequences are similar for FGM/C type I, II and III, but they tend to be more se- vere and more prevalent the more extensive the procedure (2). A systematic review (29) of the health complications of FGM/C identified a range of obstetrical problems, the most common being prolonged labour and/or obstruction, episiotomies and perineal tears, post partum haemorrhage, and maternal and foetal death. A recent study (30) investigating 28,393 women attending obstetric centres in African countries concluded that women with FGM/C were significantly more likely than those without to have adverse obstetric outcomes such as a caesarean section, infant resuscitation, and inpatient perinatal death. The authors also con- cluded that the risks seemed to be greater with more extensive FGM/C. The associa- tions were modest, however, and two studies from Sweden did not confirm a link between FGM/C and prolonged labour or perinatal death (31;32). Also the literature regarding infertility is inconclusive. While a study using DHS data from the Central African Republic, Côte d'Ivoire and Tanzania failed to confirm a statistical associa- tion between FGM/C and infertility (33), a case-control study from Sudan concluded there was a statistically as well as clinically significant association between FGM/C and primary infertility (34). 20 Background
It is possible that FGM/C performed by medical personnel in health clinics may re- duce some short term complications regularly seen when it is performed by tradi- tional practitioners. However, conditions are not necessarily sanitary or complica- tions less severe. Further, there is no evidence that medicalization reduces obstetric or other long term complications associated with FGM/C (2). Henceforth, the medi- cal profession, led by the WHO and the World Medical Association, has condemned medicalization of FGM/C (35). Other consequences Similarly to the general physical consequences of FGM/C, the impact of FGM/C on other areas of women’s health, particularly psychological, social and sexual health, has not been sufficiently investigated. Psychological consequences For many girls and women, undergoing FGM/C is a traumatic experience that may leave a lasting psychological mark and adversely affect their mental health. As an example, some researchers assert that FGM/C, representing a violation of women's physical intactness, can be classified as a "psychological trauma according to DSM- IV and a potential cause of posttraumatic stress disorder" (36). Karim (in (37)) stated that FGM/C leads to psychological disturbances and Toubia (28) explained that many infibulated women in Sudan suffer chronic anxiety and depression as a result of worry over their cut status. A qualitative study of the psychosocial impact of FGM/C among Bedouin-Arabs in Israel found that women with FGM/C expressed various emotional difficulties and psychosocial problems, including loss of trust within the mother-daughter relationship. Women reported feelings of fear, helpless- ness, and anger related to FGM/C. One said: "I perceive it as abuse" (38). Recently, Vloeberghs and colleagues (39) interviewed 66 women with various types of FGM/C. Most of the women, who lived in the Netherlands, reported a number of psychologi- cal effects from FGM/C, including anxiety, bad memories and stress. On the other hand, many women with FGM/C report feeling proud (40) and some argue FGM/C made them a better person: "I was very happy to go through it since I had been look- ing forward to it" (41). Social consequences FGM/C is a deeply entrenched social convention among some ethnic groups and as such carries consequences both when it is and when it is not practised. FGM/C can be a source of personal and collective identity, as well as power in their daily affairs, as illustrated by one Sudanese woman: "It gives women a lot of power in the house- hold" (42). When girls and families conform to the practice they acquire social posi- tion and respect. Conversely, failure to conform leads to difficulty in finding a hus- band for the girl, shame, stigmatization, as well as loss of social position, honour and protection, resulting in the family’s social exclusion in the community (35;43;44). Women from five African countries reported that FGM/C influenced their relations with their partner, children and relatives in their country of origin (39). 21 Background
Sexual consequences As stated earlier, with FGM/C, parts of the women's erogenous genital areas as well as sexually responsive vascular tissue are removed. From the above concepts of the female sexual response, it is easy to deduce that excision of women's genital parts, coupled with damaged nerve-endings and the development of scar tissue and adhe- sions around the excised parts, reduce a women's capacity for sexual enjoyment (45). It has been found that vascular tissue is important for sexual response (26). Some researchers state that the sensitivity and integrity of the clitoris and labia mi- nora are essential for experiencing sexual satisfaction (45). However, women's sexu- ality, as men's, is a complex interaction of neurophysiological and biochemical mechanisms, and influenced by relationship dynamics and family and sociocultural issues (46). It is also likely that a woman's sexuality is affected according to the ex- tent of excision and the degree to which other social messages that inhibit sexual ex- pression are internalized (28). For example, although interviews with Bedouin women in southern Israel (18) and Eritrean women (47) found that women reported pain during intercourse in the months after marriage, none felt that is was related to having been cut. On the other hand, Mukoro (48) concluded that sexual satisfaction diminished after FGM/C was performed. In this study of 46 women with FGM/C type I or II carried out in young adulthood or adolescence, the majority of the women (63%) had satisfactory sexual relationships before being cut, but this dropped to 8.7% after being cut. A few other studies report on sexual arousal and experiences. Reyners (49) referring to a study among 2000 Egyptian women, summarized that 25% of women with FGM/C did not feel any arousal during intercourse, 50% experienced pain during intercourse, and 56% never experienced orgasm. Among participants in Ghana (50) 46% reported they did not enjoy sex and 41% said sex was associated with pain. In contrast, among 195 immigrated women in northern Europe, 90% of adult women with FGM/C reported that sex gave them pleasure and 69% always experienced or- gasm (51). Also results from qualitative studies show a spectrum of experiences. Lightfoot-Klein (52) found that the majority of her infibulated Sudanese interview- ees experienced sexual desire, pleasure and orgasm. Johnsdotter and Essen (53) re- ported that most of their respondents stated they did not have sexual problems and enjoyed sexual relations. Johansen (54) found that a little more than half of the fe- male Somali respondents complained of reduced sexual feelings from FGM/C. This variation was evident also in Abusharaf's study (42): For example, one woman stated "My infibulations did not eliminate my desire to have sex even at this age" while another said "I have to tell the truth: infibulating does not allow women to want sex." Among Eritrean interviewees, sexual satisfaction came from being in tune with their partner and having a loving relationship (47). In the mid 1990s, Toubia (28) concluded that little scientific research was available on the sexual consequences of FGM/C, and Obermeyer's review (55) a few years later confirmed that only a handful of studies existed. Until now, the researcher's 22 Background
updated review of the consequences of FGM/C for health and sexuality may have represented the best available evidence regarding the sexual sequelae of FGM/C. The review included 35 sources and the results with respect to sexuality were sum- marized: "while one study … reports that circumcised women are significantly more likely to suffer adverse consequences for sexual enjoyment, other studies that meas- ure sexual activity and pleasure find no significant difference between circumcised and uncircumcised women" (56). Obermeyer concluded that most of the existing studies suffered from conceptual and methodological shortcomings, and the avail- able evidence did not support the hypotheses that FGM/C destroys sexual function- ing or precludes enjoyment of sexual relations. Presently, there are no systematic reviews of the impact of FGM/C on women’s psy- chological, social and sexual health. Thus, the aim of this systematic review was to summarize published, empirical data describing the psychological, social and sexual consequences of FGM/C. We believe a systematic review on this topic is important for several reasons. A systematic review provides a more precise estimate of conse- quences than is possible from individual, primary studies. It can form the basis of evaluating current practice as well as highlighting gaps and uncertainties in current research knowledge, and thus the research questions that need to be addressed in subsequent studies. 23 Background
Method
We conducted a systematic review of the psychological, social and sexual conse-
quences of FGM/C in accordance with the NOKC handbook for summarizing evi-
dence (57) and most of the guidelines in the Cochrane Handbook for Systematic Re-
views of Interventions (58).
LITERATURE SEARCH
The database search strategy was designed and executed February 4-9 2009, and
repeated in February 2010, by research librarian Sari Ormstad at NOKC. The search
in Anthropology Plus was executed February 19 2009, by Hege Oswald at NKVTS.
We searched systematically for relevant literature in the following 13 international
databases:
• African Index Medicus
• Anthropology Plus
• British Nursing Index and Archive
• The Cochrane Library (CENTRAL, Cochrane Database of Systematic Reviews,
Database of Abstracts of Reviews of Effects)
• EMBASE
• EPOC
• MEDLINE
• PILOTS
• POPLINE
• PsycINFO
• Social Services Abstracts
• Sociological Abstracts
• WHOLIS
The strategy incorporated subject headings (for example MeSH terms in MEDLINE)
and text words (in title and abstract) relating to FGM/C and the four classifications
thereof, such as mutilation, circumcision, excision. No method filters were applied
as we were more concerned about sensitivity than specificity. The complete search
strategy is detailed in Appendix 1. We supplemented the database search with
searches in databases of six international organizations that are engaged in projects
regarding FGM/C (see Appendix 1), as well as searches in reference lists of relevant
24 Methodreviews and included studies. Additionally, we communicated with experts engaged
in FGM/C related work. Unpublished reports, abstracts, brief and preliminary re-
ports were considered for inclusion on the same basis as published reports.
INCLUSION CRITERIA
We accepted several study designs:
1. systematic reviews,
2. cohort studies,
3. case-control studies,
4. cross-sectional studies.
Population: Girls and women who had been subjected to any type of FGM/C, as
classified by the WHO (2).
Interest: FGM/C classified as type I to type IV according to the WHO modified
typology (2).
Comparison: Girls and women who had not been subjected to any type of FGM/C,
as defined by the WHO (2).
Outcomes: Psychological, social and sexual consequences of FGM/C, including
but not limited to anxiety, post traumatic stress syndrome, school ab-
senteeism, sexual satisfaction, libido and dyspareunia (pain during
intercourse). The focus was behavioural and experiential conse-
quences in the three interest areas psychological, social and sexual
consequences.
We enforced no limitations on age, race/ethnicity, nationality or other participant
characteristics. The women needed to be part of a community in which FGM/C was
a customary practice. We included all publication years and languages. When con-
sidered likely to meet the inclusion criteria, studies were translated to English.
In sum, studies eligible for the review were those that as a minimum compared two
groups of females (girls/women with FGM/C vs girls/women without FGM/C) with
respect to a quantitatively measured psychological, social or sexual outcome.
EXCLUSION CRITERIA
We excluded all studies not meeting our pre-specified inclusion criteria. Specifically,
we excluded non-systematic reviews, qualitative studies, quantitative studies that
did not compare women with FGM/C to women without FGM/C. With respect to
outcomes, we excluded studies without a quantitative measure of a psychological,
social or sexual outcome.
25 MethodSELECTION OF STUDIES Two authors (Berg and Denison) independently read all titles/and or abstracts re- sulting from the search process. We compared our judgements and eliminated any obviously irrelevant publications. Next, we obtained full text copies of the potentially relevant studies (two records could not be obtained in full text). The same pair of authors, acting independently, classified the studies read in full text as relevant, that is, met all inclusion criteria and therefore to be included, or irrelevant and therefore to be excluded. We then compared our judgements and excluded studies that did not meet all inclusion criteria. Pre-designed inclusion/exclusion forms were used for each screening level. It was not necessary to contact the authors of any studies to aid the decision process. Decisions were made on inclusion criteria outlined, i.e. types of studies, types of par- ticipants, comparison groups, and outcome measures used. Differences in opinion in the screening process were few and were resolved through consensus. Studies for- mally considered in full text but excluded are listed in Appendix 2 and reasons for exclusion are provided. DATA EXTRACTION AND ANALYSIS Two authors independently extracted data from the published sources using a pre- designed data recording form. Where differences in data extracted occurred, this was resolved by re-examination of the publication and subsequent discussion. With respect to quality of included studies, we used an adapted version of the NOKC quality assessment tool for cross-sectional studies. Given our focus on consequences of exposure to FGM/C, the assessment tool was modified by the addition of five questions from the NOKC quality assessment tool for cohort studies in order to cap- ture whether a) the compared groups (women with FGM/C and women without FGM/C) were selected from the same population; b) the groups were comparable with respect to important backgrounds factors; c) exposure and outcome were measured in the same way in the two groups; d) the person who assessed the out- come was blind to whether participants were exposed or not; and e) known, poten- tially important confounders had been considered in the study design and/or analy- ses. The adapted check list with its 12 questions is listed in Appendix 3, including our assessment of each question. Berg and Denison agreed upon a final decision of strong, moderate or weak methodological quality for each study after discussing whether there was a discrepancy between the two reviewers with respect to the ques- tions. We applied this assessment tool for all included studies (cross-sectional and case-control studies). 26 Method
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